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Open AcceResearch articleVariation in incidence of breast, lung and cervical cancer and malignant melanoma of skin by socioeconomic group in EnglandLorraine Shack*1,2, Catrina Jordan3, Catherine S Thomson4, Vivian Mak5, Henrik Møller2,5 for UK Association of Cancer Registries
Address: 1North West Cancer Intelligence Service, Christie Hospital NHS Trust, Kinnaird Road, Withington, Manchester, M20 4QL, UK, 2Non-communicable Disease and Epidemiology Unit, London School of Hygiene and Tropical Medicine, WC1E 7HT, UK, 3Trent Cancer Registry, 5 Old Fulwood Road, Sheffield, S10 3TG, UK, 4Cancer Research UK, London, WC2A 3PX, UK and 5King's College London, Thames Cancer Registry, 1st Floor, Capital House, 42 Weston Street, London, SE1 3QD, UK

Email: Lorraine Shack* - [email protected]; Catrina Jordan - [email protected]; Catherine S Thomson - [email protected]; Vivian Mak - [email protected]; Henrik Møller - [email protected]

* Corresponding author

AbstractBackground: Cancer incidence varies by socioeconomic group and these variations have been linked withenvironmental and lifestyle factors, differences in access to health care and health seeking behaviour. Socioeconomicvariations in cancer incidence by region and age are less clearly understood but they are crucial for targeting preventionmeasures and health care commissioning.

Methods: Data were obtained from all eight English cancer registries for patients diagnosed between 1998 and 2003,for all invasive cases of female breast cancer (ICD-10 code C50), lung cancer (ICD-10 codes C33-C34), cervical cancer(ICD-10 code C53), and malignant melanoma of the skin (ICD-10 code C43). Socioeconomic status was assigned to eachpatient based on their postcode of residence at diagnosis, using the income domain of the Index of Multiple Deprivation2004. We analysed the socioeconomic variations in the incidence of breast, lung and cervical cancer and malignantmelanoma of the skin for England, and regionally and by age.

Results: Incidence was highest for the most deprived patients for lung cancer and cervical cancer, whilst the oppositewas observed for malignant melanoma and breast cancer. The difference in incidence between the most and the leastdeprived groups was higher for lung cancer patients aged under 65 at diagnosis than those over 65 at diagnosis, whichmay indicate a cohort effect. There were regional differences in the socioeconomic gradients with the gap being widestfor lung and cervical cancer in the North (North East, North West and Yorkshire and Humberside) and for malignantmelanoma in the East and South West. There were only modest variations in breast cancer incidence by region. If theincidence of lung and cervical cancer were decreased to that of the least deprived group it would prevent 36% of lungcancer cases in men, 38% of lung cancer cases in women and 28% of cervical cancer cases. Incidence of breast cancerand melanoma was highest in the least deprived group, therefore if all socioeconomic groups had incidence rates similarto the least deprived group it is estimated that the number of cases would increase by 7% for breast cancer, 27% formelanoma in men and 29% for melanoma in women.

Conclusion: National comparison of socioeconomic variations in cancer incidence by region and age can provide anunbiased basis for public health prevention and health commissioning. Decreasing inequalities in incidence requires theintegration of information on risk factors, incidence and projected incidence but targeted public health interventionscould help to reduce regional inequalities in incidence and reduce the future cancer burden.

Published: 26 September 2008

BMC Cancer 2008, 8:271 doi:10.1186/1471-2407-8-271

Received: 26 November 2007Accepted: 26 September 2008

This article is available from: http://www.biomedcentral.com/1471-2407/8/271

© 2008 Shack et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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BackgroundIncidence for many cancers varies by socioeconomicgroup in the UK [1-3] and other countries [4-6]. Socioeco-nomic variations have been attributed to environment[7], lifestyle [8,9], biological effects [10], access to healthcare [11-17] and health seeking behaviour [18-21]. Thesevariations are particularly wide for the cancers under study(breast, cervix, lung, malignant melanoma) due to theclose association between socioeconomic status and riskfactors. Inequalities in mortality[22] and survival [5,23-30] have been evaluated to assess improvements in ineq-uities in outcome and access to treatment. National com-parison of socioeconomic variations in cancer incidenceby region and age are less understood but provide anunbiased basis for prevention and commissioning. Previ-ous studies have focused on regional variations [22,31]with one recent study of regional and socioeconomic var-iation in breast and lung cancer[32], although this did notinclude age variations. This study aims to investigatesocio-economic differences in breast, lung, cervical andmalignant melanoma cancer incidence among patientsdiagnosed in England during 1998–2003, by region andage.

MethodsData were obtained from all eight English cancer registriesfor patients diagnosed between 1998 and 2003, for allinvasive cases of female breast cancer (ICD-10 code C50),lung cancer (ICD-10 codes C33-C34), cervical cancer(ICD-10 code C53), and malignant melanoma of the skin(ICD-10 code C43). These cancer sites were selected dueto their association with risk factors closely linked to soci-oeconomic status, such as smoking, UV exposure, HPVinfection and reproductive factors. Breast and cervical can-cer were of specific interest due to socioeconomic varia-tions in screening up-take.

A socioeconomic group was assigned to each patientbased on their postcode of residence at diagnosis, usingthe income domain of the Index of Multiple Deprivation2004 (IMD) [33]. IMD is a national measure of depriva-tion for each Lower Super Output Area in England basedon information collected at census and in governmentdatabases, such as income support and job seekers allow-ance. IMD is based on seven domains of deprivation(income, employment, health deprivation and disability,education skills and training, barriers to housing and serv-ices, crime and living environment). To exclude the healthrelated measures of the IMD, only the income domain ofthe IMD was used in this study. This has been shown tostrongly correlated with deprivation and exclude healthrelated measures [25,34]. The national income domain ofthe IMD for all lower super output areas (LSOAs) in Eng-land was ranked in ascending order and divided intoquintiles, each containing 20% of the total population of

England [35], with quintile 1 being least deprived fifth ofthe population and quintile 5 the most deprived fifth ofpopulation. Super output areas are geographies that wereintroduced by the Office for National Statistics (ONS) inand attempt to create a uniform geographic system acrossEngland for analysis that stays stable over time. There are32,482 lower super output areas (LSOAs) in England withan average population size of 1,500 residents [36].

European age-standardised incidence rates (ASRs) werecalculated by deprivation quintile, cancer site, Govern-ment Office Region (GOR) (Figure 1), age group (under65, 65 and over) and gender. Rate Ratios (RR) were calcu-lated by region and age (under 65 and 65 and over) usingthe least deprived (quintile 1) as the baseline. The number(and percentage) of additional/fewer incident cases thatwould be expected if incidence rates in all deprivationgroups was the same as those in the least deprived wasestimated. The difference between the observed andexpected number of cases for socioeconomic group wascalculated to provide an estimate of the burden of cancershould these inequalities change. All analyses were donein EXCEL and STATA 8.0 [37].

This study was carried out in association with the UnitedKingdom association of Cancer Registries (UKACR) whichcollect and conduct cancer surveillance using the data theycollect under Section 60 of the Health and Social Care Act2002. The study used an anonymised dataset and separateethical approval was not required.

ResultsThe highest incidence rates in England occurred in themost deprived groups for both lung cancer and cervicalcancer, while the opposite was the case for malignantmelanoma and breast cancer with the least deprivedgroups having the highest incidence (Table 1). The ine-quality between the least deprived, and the mostdeprived was highest for lung cancer in men (RR 2.5395% CI: 2.48–2.58) and women (RR 2.73 95% CI: 2.66–2.80). Similarly, cervical cancer incidence was highest inthe most deprived group (RR 2.08 95% CI: 1.97–2.19)and decreased consistently with increasing affluence. Ifall population groups has the same incidence rates as theleast deprived group, we would expect 41,076 (36%)fewer lung cancer cases in men, 28,148 (38%) fewercases in women and 4,108 (28%) fewer cervical cancercases. Breast cancer incidence was highest in the leastdeprived with modest differences between socioeco-nomic groups (Breast: RR 0.84 95% CI: 0.82–0.85).Malignant melanoma incidence showed wide variationsby socioeconomic status but similar trends for men andwomen (Melanoma in men: RR 0.49 95% CI: 0.47–0.52,Melanoma in women: RR 0.48 95% CI: 0.46–0.51). Ifthe socioeconomic-specific incidence rates where equal




Map of Regions in UKFigure 1Map of Regions in UK.


to those in the least deprived quintile across all popula-tion groups the number of breast cancer cases would riseby 15,496 (7%) and cases of malignant melanoma of theskin would increase by 4,286 (27%) in men and 5,862(29%) in women.

There were only modest differences in socioeconomic-specific breast cancer incidence rates both between andwithin regions, with the highest in the East Midlands (RR0.89 95% CI 0.85–0.94) and the lowest in London (RR0.79 95% CI 0.76–0.83) (Figure 2). Socioeconomic varia-tions by age were small and not significantly different forwomen aged under 65 and over 65 (Figure 3).

Cervical cancer incidence varied substantially withinregions by socioeconomic group with a large increase inincidence occurring between the second and the mostdeprived group in most regions, except London and theEast of England. This difference was most significant inthe South West with an age standardised incidence rate of10.3 per 100,000 (95% CI: 9.1–11.5) in the second mostdeprived and 15.5 per 100,000 (95% CI: 13.3–17.7) inthe most deprived group. Socioeconomic-specific inci-dence rates in general, as well as the difference betweenthe most and least deprived were lowest in London andthe East of England. In contrast the highest incidence rateswere recorded in deprived groups in the North West andSouth West. The gap between most and least deprived was

Table 1: Incidence by socioeconomic status for lung, breast, cervical, and melanoma cancer, England, 1998–2003

Men Women

Deprivation No. AVR RR Excess cases compared to least deprived

% Deprivation No. AVR RR Excess cases compared to least deprived

%

Lung LungLeast Deprived 15177 42.2 1.00 - Least Deprived 9024 21.1 1.00 -2 19341 51.1 1.21 -3296 2 12015 25.7 1.22 -27823 22572 52.1 1.46 -7143 3 14286 30.7 1.46 -45044 26125 79.2 1.87 -12,137 4 17246 40.5 1.92 -8281Most Deprived 30573 107.4 2.53 -18499 Most Deprived 20789 57.5 2.73 -13180Total 113788 -41076 -36.1 Total 73360 -28148 -38.4

Melanoma MelanomaLeast Deprived 4239 12.8 1.00 - Least Deprived 5217 14.8 1.00 -2 3908 11.5 0.90 425 2 4901 13.3 0.90 5393 3368 10.3 0.81 796 3 4356 11.8 0.80 10994 2571 8.5 0.67 1292 4 3506 9.9 0.67 1715Most Deprived 1724 6.3 0.49 1772 Most Deprived 2352 7.2 0.484 2509

Total 15810 4286 Total 20332 5862 28.8

Breast

Least Deprived 46085 125.7 1.00 -2 46745 121.6 0.97 15573 44718 118.1 0.94 28594 39800 112.6 0.90 4643Most Deprived 32672 105.0 0.84 2509

Total 210020 7.4

Cervix

Least Deprived 2149 6.4 1.00 -2 2515 7.2 1.13 -2893 2782 7.8 1.23 -5204 3362 9.9 1.54 -1185Most Deprived 4072 13.3 2.08 -2113

Total 14880 -4108 -27.6



greatest in the North West and Yorkshire and Humber-side. The deprivation gap was not statistically differentbetween those under 65 and 65 and over.

Incidence rates for lung cancer were 40% lower in womenthan men however the trends by age and regional were

still similar. The highest incidence rates occurred in themost deprived group for both men and women in theNorth East and North West, with the lowest occurring inthe East of England (Figure 2). The North East and WestMidlands had the highest deprivation gap in men, withthe North West and North East having the highest forwomen. Lung cancer was the only site with a significantdifference in the deprivation gap by age group with thoseaged under 65 having a higher gap (men: RR 3.29 95% CI:3.16–3.41, women: RR 3.18 95% CI 3.03–3.34) thanthose age 65 and over (men: RR 2.26 95% CI 2.20–2.30and women: RR 2.29 95% CI 2.42–2.56) (Figure 4).

The deprivation gap for malignant melanoma was similarin men and women, with the exception of the North Eastwhere it was larger in men, and the South West, where itis larger in women. Incidence was higher for each socioe-conomic group and the deprivation gap narrower in theSouth West than in other regions, for both men (RR 0.8495% CI: 0.70–1.00) and women (RR 0.69 95% CI: 0.58–0.81). In the North East there was some inconsistency insocioeconomic-specific incidence for malignantmelanoma as incidence in the second least deprivedgroup had lower incidence than the socioeconomicgroups on either side. London had the lowest incidence

Breast cancer incidence (European age-standardised rate per 100,000) by Government Office Region, England, 1998–2003Figure 2Breast cancer incidence (European age-standardised rate per 100,000) by Government Office Region, England, 1998–2003.

20

40

60

80

100

120

140

North East North West Yorkshire &Humber

East Midlands West Midlands East of England London South East South West

Government Office Region

EA

SR

affluent 2 3 4 deprived

Lung cancer incidence in men (European age-standardised rate per 100,000) by Government Office Region, England, 1998–2003Figure 3Rate ratio for cancer incidence for patients in least to most deprived socioeconomic group, England, 1998–2003.

0

1

2

3

4

Melanom a (m en) Melanoma (wom en) Lung (m en) Lung (wom en) Breas t Cervix

Rat

e ra

tio

under 65

65 and over



for all deprivation groups, in men and women. The largestdifference between least and most deprived occurred inWest Midlands for men (RR 0.43 95% CI: 0.36–0.51) andYorkshire and Humber for women (RR 0.38 95% CI:0.32–0.44).

DiscussionSocioeconomic variations in cancer are of interest toinform public health prevention and health care plan-ning, particularly in developing programmes to reduceinequalities in health, for which there are key targets inEngland [38,38]. While survival and mortality can beinfluence in the short term cancer incidence requires thelatent period before any impacts can be evaluated. Despitethis lag time evaluations of cancer, particularly by age,region and deprivation, can assist in public health plan-ning and targeted prevention.

Women in the least deprived socioeconomic groups havehigher breast cancer incidence which has been attributedto the association of socioeconomic status with reproduc-tive factors [39] and has been seen in other studies [4,40].Women from a less deprived socioeconomic group maybe more likely to have their first child at a later age, havefewer children in their lifetime and take hormone replace-ment therapy, with each of these factors associated with

increased breast cancer incidence [39-41]. Breast cancer isassociated with obesity in post-menopausal women, withthe association particularly strong for deprived women[42]. Deprived women have lower levels of screening up-take to the national mammographic screening pro-gramme for 50 to 65 year olds (extended to 65 to 69 in2007) [43-45], however there was little variation by soci-oeconomic status. The constancy across regions and soci-oeconomic status may possibly be due to high awarenessamong all groups. The moderate variations in breast can-cer incidence and deprivation gap across regions was con-sistent with other studies by region and socioeconomicstatus, with the socioeconomic differences in incidenceremaining constant for most regions over time [32]. AScottish study of inequalities in breast cancer survivalfound the despite differential screening up-take inequali-ties in survival had narrowed in the screening ages sincethe implementation of the screening programme [46].

Cervical cancer screening began nationally in England in1988 for women aged 20 to 65 years but the age at firstscreening invitation was raised to 25 years in 2005 [47].Screening detects dysplastic lesions and in situ (CIN III)tumours that are then removed prior to developing intoinvasive cervical cancer. Most cervical cancers develop as aresult of Human Papilloma Virus (HPV), an asympto-

Rate ratio for cancer incidence for patients in least to most deprived socioeconomic group, England, 1998–2003Figure 4Lung cancer incidence in men (European age-standardised rate per 100,000) by Government Office Region, England, 1998–2003.

0

20

40

60

80

100

120

140

North East North West Yorkshire &Humber

East Midlands West Midlands East ofEngland

London South East South West

Government Office Region

EA

SR

affluent 2 3 4 deprived



matic sexually transmitted infection which is carcino-genic. HPV infection is associated with younger age andhigher number of partners [48-50], after adjusting forthese factors socioeconomic status was associated withHPV infection in some studies [48,49] while others foundno significant association [50]. Screening up-take hasbeen reported to vary by socioeconomic status [51] and belower for women with low levels of education in England[52]. The lower incidence rates of cervical cancer forSouthern England (East, South West, London and SouthEast) are consistent with other national studies [31]. Soci-oeconomic-variations in screening up-take contribute tothe regional variations in deprivation gap, although theregional variations and influence of HPV infection (andassociated risk factors) remains an area for further study.

The high lung cancer incidence and deprivation gap inthis study is consistent with other studies [31,32]. Smok-ing is strongly associated with socioeconomic status withover 80% of lung cancer cases are estimated to be attribut-able to smoking [53,54]. Smoking prevalence rapiddecreased during the 1970s and 1980s, with largerdecreases occurring in the non-manual groups [55] whichis consistent with an increase in the deprivation differ-ences found in other studies [32]. Smoking prevalence in2006 was higher in the manual occupational groups(27%) than the non-manual groups (17%)[56]. Manualgroups were also associated with higher tobacco con-sumption and beginning smoking at an earlier age [56].Smoking prevalence by socioeconomic status is not cur-rently available. While occupational and socioeconomicstatus can not be directly compared evidence suggests thatthe manual occupational groups are more similar to themore deprived, than the least deprived.

The large deprivation-specific differences found in inci-dence rates for patients diagnosed with lung cancer under65, may indicate a cohort effect. In contrast to older ageswhere rapid decreases in smoking occurred during the1970s and 1980s there have been larger decreases in theproportion of young men smoking than young women[55,56]. A large cross-sectional study of socioeconomicgradients in smoking among young women in Southamp-ton, England found the prevalence of smoking was high-est among the most deprived [57] with the socioeconomicdifferences increasing with age, as smoking cessation wasmore common in the least deprived. These trends maysuggest a cohort effect with continuing inequalities inlung cancer incidence by age, continued monitoring ofsmoking prevalence is key to assessing these. In June 2007a national smoking ban in enclosed public spaces wasintroduced, it remains to be seen if this will decreasesmoking prevalence and/or tobacco consumption.

Incidence of malignant melanoma of the skin in Englandis expected to increase by 88% in men (66% in women)

by 2020 [58], with regional variations in these increases[59]. Regional variations in skin cancer have also beenseen in other countries with variations attributed to UVexposure and opportunities for recreational exposure [60-62]. Within the UK the South West receives the most UVexposure [49] and also has an older population with bothcontributing to the high incidence of malignantmelanoma. Exposure to UV has increasingly occurredthrough sun bed use and holidays abroad which are bothsignificantly associated with malignant melanoma [60].Higher incidence in the least deprived and regional varia-tions may be largely explained by holidays abroad andexposure to natural UV, however current UV exposurehighlights changes to these trends. It is difficult to esti-mate sun bed use as most are private and unregulatedhowever, anecdotal evidence suggests that sun bed use isincreasing in England particularly for teenagers and youngadults and may represents a cohort of individuals athigher risk in the future. Exposure to sunbeds before theage of 35 was increased the risk of malignant melanomaby 75% [63]. A study in Dundee, Scotland found thenumber of sun parlours has increased by up to 30% since1998 and that 83% of the sun beds exceeded the Euro-pean standard for UV(B) radiation levels [64]. There isincreasing access to sun beds through private unmannedsun parlours, with sun parlours tending to be clustered inareas of deprivation [65]. The cohort of high risk individ-uals may represent a substantial burden of future skincancer.

Cancer registries in England collect data to a national spec-ification and have high levels of case ascertainment andconsistency [66]. However, there is probably some regionalvariation due to differences in data collection and timeli-ness, although this is unlikely to explain the magnitude ofdifferences. Completeness of registration information, suchas treatment and stage is known to be less complete fordeprived patients [67,68]. These variations would onlyinfluence the results of this study if a patients' diagnosisdate were changed, and even in this case very little impactwould be expected due to grouping of years, however thisis unlikely due to the high quality of registry data [66].Ascertainment of lung and breast cancers are known to behigh although [69] regional variations in ascertainment ofmalignant melanoma have been shown for the early 1990s[31,70,71] with late stage tumours more likely to be regis-tered [72]. Increased use of hospital admission system datain the late 1990s and 2000s would be expected to improvedascertainment, although no direct comparison of this hasbeen published.

Ecological measures of socioeconomic status have beenwidely used by population-based cancer registries [25,34]and in the absence of individual measures of socioeco-nomic status are a pragmatic choice. As socioeconomicstatus is based on area of residence at diagnosis it may not



necessarily be representative of every patient's current orhistorical socioeconomic group and the associated cancerrisk factors. However, generally people living in the samearea have similar levels of deprivation and have found tobe robust over time [34]. This is particularly relevant forcancers where exposure to risk factors occurs years or dec-ades before cancer diagnosis. Alternative measures of soci-oeconomic status based on individual level data, such aseducation, occupation or income are also frequently usedalthough cancer registries do not routinely collect these.

ConclusionIn the long-term decreasing socioeconomic variations inincidence will have a substantial impact on the burden ofcancer, for both incidence and mortality. Variations inregional lung and cervical cancer and malignantmelanoma rates highlight variations in exposure to riskfactors. Lung cancer trends identified larger inequalities inthose under 65 at diagnosis, while there were substantialregional and age specific variations for malignantmelanoma. Socioeconomic variations in survival canpotentially be targeted more quickly while efforts tochange incidence will take many years to show any bene-ficial impact however, in the long term, decreasing ine-qualities in incidence will also decrease mortality anddecrease the number of incident cases.

AbbreviationsICD-10: International Classification of Diseases version10; LSOA: lower super output areas; IMD: Index of Multi-ple Deprivation; GOR: Government Office Region; HPV:Human Papilloma Virus; CIN III: Carcinoma in situ; UV:Ultra Violet Radiation.

Competing interestsThe authors declare that they have no competing interests.

Authors' contributionsCJ, CT, LS, HM and VM were involved in the study designwith the statistical analysis carried out by CJ and LS. LSwrote the draft of the manuscript to which all authors sub-sequently contributed. All authors contributed to theinterpretation of results and revision and approval of thefinal manuscript.

AcknowledgementsThis study was supported by UK Association of Cancer Registries and its constituent cancer registries for whom the authors were employed. The authors would like to thank the UKACR for data collection, study design, comments on the draft and decision to submit. The authors would also like to thank Lucy Boyd, Epidemiologist at Cancer Research UK for providing some of the references and Holger Möller, Intelligence Project Officer at NWCIS for his comments.

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